Skip to main content
Log in

Evolution of structure and function of V-ATPases

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Proton pumping ATPases/ATPsynthases are found in all groups of present-day organisms. The structure of V- and F-type ATPases/ATP synthases is very conserved throughout evolution. Sequence analysis shows that the V- and F-type ATPases evolved from the same enzyme already present in the last common ancestor of all known extant life forms. The catalytic and noncatalytic subunits found in the dissociable head groups of the V/F-type ATPases are paralogous subunits, i.e., these two types of subunits evolved from a common ancestral gene. The gene duplication giving rise to these two genes (i.e., encoding the catalytic and noncatalytic subunits) predates the time of the last common ancestor.

Mapping of gene duplication events that occurred in the evolution of the proteolipid, the noncatalytic and the catalytic subunits, onto the tree of life leads to a prediction for the likely subunit structure of the encoded ATPases. A correlation between structure and function of V/F-ATPases has been established for present-day organisms. Implications resulting from this correlation for the bioenergetics operative in proto-eukaryotes and in the last common ancestor are presented. The similarities of the V/F-ATPase subunits to an ATPase-like protein that was implicated to play a role in flagellar assembly are evaluated.

Different V-ATPase isoforms have been detected in some higher eukaryotes. These data are analyzed with respect to the possible function of the different isoforms (tissue specific, organelle specific) and with respect to the point in their evolution when these gene duplications giving rise to the isoforms had occurred, i.e., how far these isoforms are distributed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bennett, A. B., and Spanswick, R. M. (1984).Plant Physiol. 74, 545–548.

    Google Scholar 

  • Bernasconi, P., Rausch, T., Gogarten, J. P., and Taiz, L. (1990).FEBS Lett. 259, 227–229.

    Google Scholar 

  • Bernasconi, P., Rausch, T., Struve, I., Morgan, L., and Taiz, L. (1990).J. Biol. Chem. 265, 17428–17431.

    Google Scholar 

  • Birman, S., Meunier, F.-M., Lesbats, B., LeCair, J.-P., Rossier, J., and Israel, M. (1990).FEBS Lett. 261, 303–306.

    Google Scholar 

  • Blair, H. C., Teichelbaum, S. L., Ghiselli, R., and Gluck, S. (1989).Science 245, 855–857.

    Google Scholar 

  • Cross, R. L., and Taiz, L. (1990).FEBS Lett. 259, 227–229.

    Google Scholar 

  • Dayhoff, M. O., Schwartz, R. M., and Orcutt, B. C. (1978). InAtlas of Protein Sequence and STructure, Vol. 5, Suppl. 3 (Dayhoff, M. O., ed.), Natl. Biomedical Research Foundation, Washington DC, pp. 345–358.

    Google Scholar 

  • Denda, K., Konishi, J., Oshima, T., Date, T., and Yoshida, M. (1989).J. Biol. Chem. 264, 7119–7121.

    Google Scholar 

  • Feeley, D. E., and Deyer, J. K. (1987).J. Protozool. 34, 80–83.

    Google Scholar 

  • Felsenstein, J. (1981).J. Mol. Evol. 17, 368–376.

    Google Scholar 

  • Felsenstein, J. (1988).Phylogeny Inference Package, Version 3.2 and 3.3, Department of Genetics SK-50, University of Washington, Seattle, Washington 98195.

    Google Scholar 

  • Feng, D., and Doolittle, R. F. (1987).J. Mol. Evol. 25, 351.

    Google Scholar 

  • Fillingame, R. H. (1990). InThe Bacteria: A Treatise on Structure and Function, Vol. 12 (Krulwich, T. A., ed.), Academic Press, New York, pp. 345–391.

    Google Scholar 

  • Fitch, W. M., and Margoliash, E. (1967).Science 15, 279–284.

    Google Scholar 

  • Forgac, M. (1989).Physiol. Rev. 69, 765–796.

    Google Scholar 

  • Foury, F. (1990).J. Biol. Chem. 265, 18554–18560.

    Google Scholar 

  • Gluck, S., and Cadwell, J. (1987).J. Biol. Chem. 262, 15780–15787.

    Google Scholar 

  • Gogarten, J. P., Kibak, H., Taiz, L., Bowman, E. J., Bowman, B. J., Manolson, M. F., Poole, R. J., Date, T., Oshima, T., Konishi, J., Denda, K., and Yoshida, M. (1989a).Proc. Natl. Acad. Sci. USA,86, 6661–6665.

    Google Scholar 

  • Gogarten, J. P., Rausch, T., Bernasconi, P., Kibak, H., and Taiz, L. (1989b).Z. Naturforsch. 44c 641–650.

    Google Scholar 

  • Hanada, H., Hasebe, M., Moriyama, Y., Maeda, M., and Futai, M. (1991).Biochem. Biophys. Res. Commun. 176, 1062–1067.

    Google Scholar 

  • Hensel, R., Demharter, W., Kandler, O., Kroppenstedt, M., and Stackebrandt, E. (1986).Int. J. Sys. Bacteriol. 36, 444–453.

    Google Scholar 

  • Hensel, R., Zwickl, P., Fabry, S., Lang, G., and Palm, P. (1989).Can. J. Microbiol. 35, 81–85.

    Google Scholar 

  • Hoppe, J., and Sebald, W. (1984). The proton conducting Fo-part of bacterial ATP synthases,Biochim. Biophys. Acta 768, 1–27.

    Google Scholar 

  • Ihara, K., and Mukohata, Y. (1991).Arch. Biochem. Biophys. 286, 111–116.

    Google Scholar 

  • Inatomi, K.-I., Eya, S., Maeda, M., and Futai, M. (1989).J. Biol. Chem. 264, 10954–10959.

    Google Scholar 

  • Iwabe, N., Kuma, K.-I., Hasegawa, M., Osawa, S., and Miyata, T. (1989).Proc. Natl. Acad. Sci. USA 86, 9355–9359.

    Google Scholar 

  • Iwabe, N., Kuma, K.-I., Kishino, H., Hasegawa, M., and Miyata, T. (1991).J. Mol. Evol. 32, 70–78.

    Google Scholar 

  • Kakinuma, Y., and Igarishi, K. (1990).FEBS Lett. 271, 97–101.

    Google Scholar 

  • Kakinuma, Y., Igarishi, K., Konishi, K., and Yamato, I., (1991).FEBS Lett. 292, 64–68.

    Google Scholar 

  • Lai, S., Watson, J. C., Hansen, J. N., and Sze, H. (1991).J. Biol. Chem. 266, 16078–16084.

    Google Scholar 

  • Lake, J. A. (1991).Trends Biochem. Sci. 16, 46–50.

    Google Scholar 

  • Laubinger, W., Dimroth, P. (1987).Eur. J. Biochem. 168, 475–480.

    Google Scholar 

  • Lindmark, D. G. (1988).Exp. Parsitol. 65, 141–147.

    Google Scholar 

  • Linkkila, T. P., and Gogarten, J. P. (1991).Trends Biochem. Sci. 16, 287–288.

    Google Scholar 

  • Mandel, M., Moriyama, Y., Hulmes, J. D., Pan, Y.-C. E., Nelson, H., and Nelson, N. (1988).Proc. Natl. Acad. Sci. USA 85, 5521–5524.

    Google Scholar 

  • Meagher, L., McLean, P., and Finbow, M. E. (1990).Nucleic Acids Res. 18, 6712–6712.

    Google Scholar 

  • Mitchell, P. (1976).Biochem. Soc. Trans. 4, 399–430.

    Google Scholar 

  • Mukohata, Y., Ihara, K., Kishino, H., Hasegawa, M., Iwabe, N., and Miyata, T. (1990).Proc. Jpn. Acad. 66, 63–67.

    Google Scholar 

  • Nanney, D. L., Mobley, D. O., Preparata, R. M., Meyer, E. B., and Simon, E. M. (1991).J. Mol. Evol. 32, 316–327.

    Google Scholar 

  • Needleman, S. B., and Wunsch, C. D. (1970).J. Mol. Biol. 48, 443–453.

    Google Scholar 

  • Nelson, H., and Nelson, N. (1989).FEBS Lett. 247, 147–153.

    Google Scholar 

  • Nelson, H., Nelson, N. (1990).Proc. Natl. Acad. Sci. USA 87, 3503–3507.

    Google Scholar 

  • Nolta, K. V., Padh, H., and Steck, T. L. (1991).J. Biol. Chem. 266, 18318–18323.

    Google Scholar 

  • Pearson, W. R., and Lipman, D. J. (1988).Proc. Natl. Acad. Sci. USA 85, 2444–2448.

    Google Scholar 

  • Pedersen, P. L., and Carafioli, E. (1987).Trends Biochem. Sci. 12, 146–150, 186–189.

    Google Scholar 

  • Puhler, G., Leffers, H., Gropp, F., Palm, P., Klenk, H. P., Lottspeich, F., Garrett, R. A., and Zillig, W. (1989).Proc. Natl. Acad. Sci. USA 86, 4569–4573.

    Google Scholar 

  • Schäfer, G., Anemüller, S., Moll, R., Meyer, W., and Lübben, M. (1990).FEMS Microbiol. Rev. 75, 335–348.

    Google Scholar 

  • Sogin, M., Gunderson, J. H., Elwood, H. J., Alonso, R. A., and Peatie, D. A. (1989).Science 243, 75–77.

    Google Scholar 

  • Starke, T., Linkkila, T. P., and Gogarten, J. P. (1991).Z. Naturforsch. 46c, 613–620.

    Google Scholar 

  • Südhoff, T. C., Fried, V. A., Stone, D. K., Johnston, P. A., and Xie, X.-S. (1989).Proc. Natl. Acad. Sci. USA 86, 6067–6071.

    Google Scholar 

  • Taylor, W. R., and Green, N. M. (1989).Eur. J. Biochem. 179, 241–248.

    Google Scholar 

  • Tsutsumi, S., Denda, K., Yokoyama, K., Oshima, T., Datd, T., and Yoshida, M. (1991).Biochim. Biophys. Acta 1098, 13–20.

    Google Scholar 

  • Umemoto, N., Yoshihisa, T., Hirata, R., and Anraku, Y. (1990).J. Biol. Chem. 265, 18447–18453.

    Google Scholar 

  • Vogler, P. A., Homma, M., Irkura, V. M., and MacNab, R. M. (1991).J. Bacteriol 173, 3564–3572.

    Google Scholar 

  • Woese, C. R. (1987).Microbiol. Rev. 51, 221–271.

    Google Scholar 

  • Ying, C., Scoffone, F., Albertini, A. M., Galizzi, A., and Ordal, G. W. (1991).J. Bacteriol. 173, 3584–3586.

    Google Scholar 

  • Yokoyama, K., Oshima, T., and Yoshida, M. (1990).J. Biol. Chem. 265, 21946–21950.

    Google Scholar 

  • Yoshimi, K., and Kazuei, I. (1990).FEBS Lett. 271, 102–105.

    Google Scholar 

  • Zimniak, L., Dittrich, P., Gogarten, J. P., Kibak, H., and Taiz, L. (1988).J. Biol. Chem. 263, 9102–9112.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kibak, H., Taiz, L., Starke, T. et al. Evolution of structure and function of V-ATPases. J Bioenerg Biomembr 24, 415–424 (1992). https://doi.org/10.1007/BF00762534

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00762534

Key words

Navigation